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Codon Usage Heterogeneity in the Multipartite Prokaryote Genome: Selection-Based Coding Bias Associated with Gene

J L López1, M J Lozano1, A Lagares2,3

  • 1IBBM-Instituto de Biotecnología y Biología Molecular, CONICET, CCT-La Plata, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, La Plata, Argentina.

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Summary

Prokaryotic genomes evolve with varying codon usage adaptations across different replicons. Core chromosomal genes show gradual adaptation, unlike less adapted singletons, revealing a new strategy for bacterial fitness.

Keywords:
codon usagegenome evolutionhost-microbe interactionmobile genetic elementsplasmidome

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Area of Science:

  • Evolutionary genomics
  • Prokaryotic biology
  • Bioinformatics

Background:

  • Prokaryotes, as ancestral unicellular organisms, offer insights into genome evolution.
  • Multipartite bacterial genomes, like that of *Sinorhizobium meliloti*, present unique opportunities to study gene integration and evolution across different replicons.
  • Gene expression levels influence codon usage adaptation in highly expressed genes, such as ribosomal and translation-related proteins.

Purpose of the Study:

  • To investigate functional variations and gene evolution within the multipartite genome of *Sinorhizobium meliloti*.
  • To analyze codon usage patterns across different genomic entities (chromosome, chromid, megaplasmid, accessory plasmids) and their evolutionary implications.
  • To identify genome-wide codon usage adaptation strategies beyond ribosomal and translation-related proteins.

Main Methods:

  • Sequencing and analysis of accessory plasmid DNA.
  • Comparative genomic analysis of multiple *Sinorhizobium meliloti* genomes.
  • Correspondence analysis to assess codon usage adaptation relative to translational machinery.

Main Results:

  • Distinct functional profiles were identified for each genomic entity in *Sinorhizobium meliloti*.
  • The megaplasmid (pSymA) showed significant interstrain variation and a high density of unique genes (singletons) with plasmidome-like codon usage.
  • Codon usage adaptation to translational machinery increased from plasmidome to pSymA, pSymB, and chromosome, reflecting replicon ancestry; core chromosomal genes exhibit gradual adaptation.

Conclusions:

  • Codon usage adaptation is not limited to highly expressed genes but extends genome-wide, representing a previously undiscovered adaptation strategy for bacterial fitness.
  • Singleton genes, including those on plasmids, represent a gene pool with less ameliorated codon usage compared to more adapted genes.
  • The study presents a comprehensive model of inter- and intra-replicon heterogeneity in codon usage within a complex prokaryotic genome, highlighting evolutionary dynamics.